Arctic marine fungi: biomass, functional genes, and putative ecological roles.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
06 2019
06 2019
Historique:
received:
22
09
2018
accepted:
22
01
2019
revised:
06
01
2019
pubmed:
13
2
2019
medline:
23
11
2019
entrez:
13
2
2019
Statut:
ppublish
Résumé
Recent molecular evidence suggests a global distribution of marine fungi; however, the ecological relevance and corresponding biological contributions of fungi to marine ecosystems remains largely unknown. We assessed fungal biomass from the open Arctic Ocean by applying novel biomass conversion factors from cultured isolates to environmental sterol and CARD-FISH data. We found an average of 16.54 nmol m
Identifiants
pubmed: 30745572
doi: 10.1038/s41396-019-0368-1
pii: 10.1038/s41396-019-0368-1
pmc: PMC6775997
doi:
Substances chimiques
Fungal Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1484-1496Références
Berbee ML, James TY, Strullu-Derrien C. Early diverging fungi: diversity and impact at the dawn of terrestrial life. Annu Rev Microbiol. 2017;71:41–60.
doi: 10.1146/annurev-micro-030117-020324
Blackwell M. The fungi: 1, 2, 3…5.1 million species? Am J Bot. 2011;98:426–38.
doi: 10.3732/ajb.1000298
Hawksworth DL, Lucking R. Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr. 2017. https://doi.org/10.1128/microbiolspec.FUNK-0052-2016 .
Jones EBG, Suetrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA, et al. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers. 2015;73:1–72.
doi: 10.1007/s13225-015-0339-4
Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS, Meyer AF, et al. Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci USA. 2009;106:18315–20.
doi: 10.1073/pnas.0907303106
Comeau AM, Vincent WF, Bernier L, Lovejoy C. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci Rep. 2016;6:30120.
Rojas-Jimenez K, Wurzbacher C, Bourne EC, Chiuchiolo A, Priscu JC, Grossard HPl. Early diverging lineages within Cryptomyocta and Chytridiomyocta dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Sci Rep. 2017;7:1.
doi: 10.1038/s41598-017-15598-w
Hassett BT, Gradinger R. Chytrids dominate Arctic marine fungal communities. Environ Microbiol. 2016;18:2001–9.
doi: 10.1111/1462-2920.13216
Bochdansky AB, Clouse MA, Herdl GJ. Eukaryotic microbes, principally fungi and Labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J. 2017;11:362–73.
doi: 10.1038/ismej.2016.113
Rämä T, Hassett BT, Bubnova E. Arctic marine fungi: from filaments and flagella to operational taxonomic units and beyond. Bot Mar. 2017;60:433–52.
doi: 10.1515/bot-2016-0104
Bluhm BA, Kosobokova KN, Carmack EC. A tale of two basins: an integrated physical and biological perspective of the deep Arctic Ocean. Prog Oceanogr. 2015;139:89–121.
doi: 10.1016/j.pocean.2015.07.011
Hansell DA, Kadko D, Bates NR. Degradation of terrigenous dissolved organic carbon in the Western Arctic Ocean. Sci. 2004;304:858–61.
Neff JC, Finlay JC, Zimov SA, Davydov SP, Carrasco JJ, Schuur EAG, et al. Seasonal changes in the age and structure of dissolved organic carbon in Siberian rivers and stream. Geophys Res Lett. 2006;33:L23401.
doi: 10.1029/2006GL028222
Dashtban M, Schraft H, Syed TA, Qin W. Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Bio. 2010;1:36–50.
Wotton RS, Malmqvist B. Feces in aquatic ecosystems: feeding animals transform organic matter into fecal pellets, which sink or are transported horizontally by currents; these fluxes relocate organic matter in aquatic ecosystems. Bioscience. 2001;51:537–44.
doi: 10.1641/0006-3568(2001)051[0537:FIAE]2.0.CO;2
Turner JT. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceaogr. 2015;130:205–48.
doi: 10.1016/j.pocean.2014.08.005
Richardson MJ. Diversity and occurrence of coprophilous fungi. Mycol Res. 2001;105:387–402.
doi: 10.1017/S0953756201003884
Hassett BT, Ducluzeau AL, Collins RE, Gradinger R. Spatial distribution of aquatic marine fungi across the western Arctic and sub-Arctic. Environ Microbiol. 2017;19:475–84.
doi: 10.1111/1462-2920.13371
Cleary AC, Soreide JE, Freese D, Neihoff B, Gabrielsen TM. Feeding by Calanus glacialis in a high arctic fjord: potential seasonal importance of alternative prey. ICES J Mar Sci. 2017;74:1937–46.
doi: 10.1093/icesjms/fsx106
Zhang T, Wang NF, Zhang YQ, Liu HY, Yu LY. Diversity and distribution of fungal communities in the marine sediments of Kongfjorden, Svalbard (High Arctic). Sci Rep. 2015;5:14524.
doi: 10.1038/srep14524
Rämä T, Davey ML, Nordén J, Halvorsen R, Blaalid R, Mathiassen GH, et al. Fungi sailing the Arctic Ocean: speciose communities in North Atlantic driftwood as revealed by high-throughput amplicon sequencing. Microb Ecol. 2016;72:295–304.
doi: 10.1007/s00248-016-0778-9
Dupont S, Lemetais G, Ferreira T, Cayot P, Gervais P, Beney L. Ergosterol biosynthesis: a fungal pathway for life on land? Evolution. 2012;66:2961–8.
doi: 10.1111/j.1558-5646.2012.01667.x
Weete JD, Abril M, Blackwell M. Phylogenetic distribution of fungal sterols. PLoS ONE. 2010;5:e10899.
doi: 10.1371/journal.pone.0010899
Mille-Lindblom C, von Wachenfeldt E, Tranvik LJ. Ergosterol as a measure of living fungal biomass: persistence in environmental samples after fungal death. J Microbiol Methods. 2004;59:253–62.
doi: 10.1016/j.mimet.2004.07.010
Medina A, Probanza A, Gutierrez Manero FJ, Azcon R. Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant grwoth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol. 2003;22:15–28.
doi: 10.1016/S0929-1393(02)00112-9
Lee C, Howarth RW, Howes BL. Sterols in decomposing Spartina alterniflora and the use of ergosterol in estimating the contribution of fungi to detrital nitrogen. Limnol Oceanogr. 1980;25:290–303.
doi: 10.4319/lo.1980.25.2.0290
Newell SY. Fungal biomass and productivity. Method Microbiol. 2001;30:357–72.
doi: 10.1016/S0580-9517(01)30053-3
Vernet M, Richardson TL, Metfies K, Nöthig EM, Peeken I. Models of plankton community changes during a warm water anomaly in Arctic waters show altered trophic pathways with minimal changes in carbon export. Front Mar Sci. 2017. https://doi.org/10.3389/fmars.2017.00160.
Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol. 2010;19:21–31.
doi: 10.1111/j.1365-294X.2009.04480.x
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.
doi: 10.1128/AEM.01541-09
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.
doi: 10.1128/AEM.01043-13
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596.
doi: 10.1093/nar/gks1219
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200.
doi: 10.1093/bioinformatics/btr381
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhu kumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.
doi: 10.1093/nar/gkh293
Pernthaler A, Pernthaler J, Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Envrion Microbiol. 2002;6:3094–101.
doi: 10.1128/AEM.68.6.3094-3101.2002
He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 2007;1:67–77.
doi: 10.1038/ismej.2007.2
Van Nostrand JD, Yin H, He Z, Zhou J. Hybridization of environmental microbial community nucleic acids by GeoChip. Methods Mol Biol. 2016;1399:183–96.
doi: 10.1007/978-1-4939-3369-3_11
Picard KT. Coastal marine habitats harbor novel early-diverging fungal diversity. Fungal Ecol. 2017;25:1–13.
doi: 10.1016/j.funeco.2016.10.006
Gessner MO, Chauvet E. Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol. 1993;59:502–7.
pubmed: 16348874
pmcid: 202134
Maier MA, Peterson TD. Enumeration of parasitic chytrid zoospores in the Columbia River via quantitative PCR. Appl Environ Microbiol. 2016;82:3857–67.
doi: 10.1128/AEM.00084-16
Letcher PM, Vélez CG, Barrantes MA, Powell MJ, Churchill PF, Wakefield WS. Ultrastructural and molecular analyses of Rhizophydiales (Chytridiomycota) isolates from North America and Argentina. Mycol Res. 2008;112:759–82.
doi: 10.1016/j.mycres.2008.01.025
Karling JS. Brazilian chytrids. VI. Rhopalophlyctis and Chytriomyces, two new chitionphilic operculate genera. Am J Bot. 1945;32:362–9.
doi: 10.1002/j.1537-2197.1945.tb05132.x
Lepelletier F, Karpov SA, Alacid E, Le Panse S, Bigeard E, Garcés E, et al. Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist. 2014;165:230–44.
doi: 10.1016/j.protis.2014.02.004
Van den Wyngaert S, Rojas-Jimenez K, Seto K, Kagami M, Grossart H-P. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. J Eukaryot Microbiol. 2018;65:870–81.
doi: 10.1111/jeu.12632
Desmond E, Gribaldo S. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukarotic feature. Genome Biol Evol. 2009;1:364–81.
doi: 10.1093/gbe/evp036
Martin-Navarro CM, Lorenzo-Morales J, Machin RP, López-Arencibia A, Garcia-Castelleno JM, de Fuentes I, et al. Inhibition of 3-hydroxy-3-methylglutaryl-coenzyme A reductase and application of statins as a novel effective therapeutic approach against Acanthamoeba infections. Antimicrob Agents Chemother. 2013;57:375–81.
doi: 10.1128/AAC.01426-12
Brumfield KM, Laborde SM, Moroney JV. A model for the ergosterol biosynthetic pathway in Chlamydomonas reinhardtii. Eur J Phycol. 2017;52:64–74.
doi: 10.1080/09670262.2016.1225318
Najile SR, Molina MC, Ruiz-Trillo I, Uttaro AD. Sterol metabolism in the filasterean Capsaspora owczarzaki has features that resemble both fungi and animals. Open Biol. 2016;6:160029.
doi: 10.1098/rsob.160029
Sumathi JC, Raghukumar S, Kasbekar DP, Raghukumar C. Molecular evidence of fungal signatures in the marine protist Corallochytrium lamacisporum and its implications in the evolutions of animals and fungi. Protist. 2006;157:363–76.
doi: 10.1016/j.protis.2006.05.003
Lepère C, Ostrowski M, Hartmann M, Zubkow MV, Scanlan DJ. In situ associations between marine photosynthetic picoeukaryotes and potential parasites—a role for fungi? Environ Microbiol Rep. 2016;8:445–51.
doi: 10.1111/1758-2229.12339
Reigstad M, Wexels Riser C, Wassmann P, Ratkova T. Vertical export of particulate organic carbon: attenuation, composition and loss rates in the northern Barents Sea. Deep-Sea Res Pt II. 2008;55:2308–19.
doi: 10.1016/j.dsr2.2008.05.007
Gutiérrez MH, Pantoja S, Tejos E, Quiñones RA. The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar Biol. 2011;158:205–19.
doi: 10.1007/s00227-010-1552-z
Wheeler PA, Gosselin M, Sherr E, Thibaultc D, Kirchman DL, Benner R, et al. Active cycling of organic carbon in the central Arctic Ocean. Nature. 1996;380:697–9.
doi: 10.1038/380697a0
Gradinger R. Sea ice algae: major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep-Sea Res Pt II. 2009;56:1201–12.
doi: 10.1016/j.dsr2.2008.10.016
Auel H, Hagen W. Mesozooplankton community structure, abundance and biomass in the central Arctic Ocean. Mar Biol. 2002;140:1013–21.
doi: 10.1007/s00227-001-0775-4
Sherr EB, Sherr BF, Fessenden L. Heterotrophic protists in the central Arctic Ocean. Deep-Sea Res Pt II. 1997;44:1665–82.
doi: 10.1016/S0967-0645(97)00050-7
Sherr EB, Sherr BF, Wheeler PA, Thompson K. Temporal and spatial variation in stocks of autotrophic and heterotrophic microbes in the upper water column of the central Arctic Ocean. Deep-Sea Res Pt I. 2003. https://doi.org/10.1016/S0967-0637(03)00031-1 .
doi: 10.1016/S0967-0637(03)00031-1
Terrado R, Medrinal E, Dasilva C, Thaler M, Vincent WF, Lovejoy C. Protist community composition during spring in an Arctic flaw lead polynya. Polar Biol. 2011;34:1901–14.
doi: 10.1007/s00300-011-1039-5
Taylor JD, Cunliffe M. Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 2016;10:2118–28.
doi: 10.1038/ismej.2016.24
Orsi W, Biddle FJ, Edgcomb V. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLOS ONE 2013;8:e56335.
doi: 10.1371/journal.pone.0056335
Ghabrial SA, Castrón JR, Jiang D, Nibert ML, Suzuki N. 50-plus years of fungal viruses. Virology. 2015;479:356–68.
doi: 10.1016/j.virol.2015.02.034
Ortega-Arbulú A-S, Pichler M, Vuillemin A, Orsi WD. Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon. Environ Microbiol. 2018. https://doi.org/10.1111/1462-2920.14469 .
Grebmeier JM, Barry JP. The influence of oceanographic processes on pelagic-benthic coupling in polar regions: a benthic perspective. J Mar Sci. 1991;2:495–518.
Jeffries TC, Curlevski NJ, Brown MV, Harrison DP, Doblin MA, Petrou K, et al. Partitioning of fungal assemblages across different marine habitats. Environ Microbiol Rep. 2016;8:235–8.
doi: 10.1111/1758-2229.12373
Sun JY, Song Y, Ma ZP, Zhang HJ, Yang ZD, Cai ZH, et al. Fungal community dynamics during a marine dioflagellate (Noctiluca scintillans) bloom. Mar Environ Res. 2017;131:183–94.
doi: 10.1016/j.marenvres.2017.10.002